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[BCG03-01] Hunting mineral-centered life from deep rocky biosphere
Keywords:Primitive life , Deep biosphere, rock-water interactions
The emergence of life is generally considered to be assisted by the power of minerals. Modern organisms are equipped with biochemical machineries that might have replaced the primitive mineral parts long time ago. Given high energetic costs to operate such sophisticated machineries, it is speculated that mineral-centered life might have been evolutionarily preserved on modern Earth where the primordial geochemistry prevails with extreme energy starvation. One of ideal places to hunt the primitive life is the deep subsurface restricted by the supply of energy-rich photosynthetic products. Granite and basalt are geologic giants that have been representative of continental and oceanic crusts since ~4.0 billion years ago. Energy-starved deep biospheres in granitic and basaltic crusts have been potentially hosting primitive life without outcompeting with biochemically sophisticated microbes.
To explore the granite biosphere, 69-million-year-old granite was investigated at a 300-m deep underground tunnel at the Mizunami Underground Laboratory. Metagenomic analysis in combination with geochemical and microbiological site characterizations revealed that anaerobic methane-oxidizing archaea are harvesting energy from magmatic methane under energy-starved conditions (Ino et al. 2018). In addition, a diverse and dominant phylum within Candidate Phyla Radiation (CPR) called Parcubacteria appears to be dominant in the deep granite biosphere. All members of CPR are represented by small genomes and cell sizes with restricted metabolic capacities, which might have been inherited from an early metabolic platform for life (Hug et al. 2016).
For the oceanic crust biosphere, the JOIDES Resolution (JR) was used to drill 13, 33.5 and 104 million-year-old basalt lava during Integrated Ocean Drilling Program (IODP) Expedition 329 that targeted life beneath the seafloor of the South Pacific Gyre (SPG). To understand the nature of rocky biosphere in oceanic crust, a new life-detection technique was successfully developed for drilled rock cores in combination with nanoscale mineralogical characterizations (see Yamashita et al. 2019 and Sueoka et al. 2019 for technical details). Basalt fractures filled with clay minerals and calcium carbonate were associated with the formation of Fe/Mg- smectite compositionally and structurally similar to saponite and/or nontronite, indicators of low-temperature basalt-water interactions. Unexpectedly, the dense colonization of microbial cells was directly imaged to exceed ~1010 cells/cm3, a range of cell density typically found in human gut. More surprisingly, the dominance of heterotrophic bacteria was indicated by analyses of DNA sequences and lipids to conclude organic matter as carbon and energy sources in subseafloor basalt.
These findings change our view of the rocky biosphere where inorganic energy sources derived from rock-water interactions are generally regarded as primary ecological importance. Given the prominence of basaltic lava and/or magmatic methane on Earth and Mars, microbial life could be habitable where subsurface igneous rocks interact with liquid water. It is also important to note that microbial presence/absence and metabolic repertories will clarify poorly characterized physicochemical properties in deep igneous rocks such as permeability and fluid and energy fluxes. Finally, the technology is ready to hunt mineral-centered life in the deep subsurface for unveiling the life’s story from the very beginning.
REFERENCES
Hug, L. et al. (2016) Nature Microbiology 1, Article number: 16048.
Ino et al. (2018) ISME Journal 12: 31-47
Yamashita, S. et al. (2019) Scientific Reports 9, Article number 11306.
Sueoka, Y. et al. (2019) Frontiers in Microbiology, doi: 10.3389/fmicb.2019.02793.
Suzuki, Y. et al. (2020) Communications Biology, doi: 10.1038/s42003-020-0860-1.
To explore the granite biosphere, 69-million-year-old granite was investigated at a 300-m deep underground tunnel at the Mizunami Underground Laboratory. Metagenomic analysis in combination with geochemical and microbiological site characterizations revealed that anaerobic methane-oxidizing archaea are harvesting energy from magmatic methane under energy-starved conditions (Ino et al. 2018). In addition, a diverse and dominant phylum within Candidate Phyla Radiation (CPR) called Parcubacteria appears to be dominant in the deep granite biosphere. All members of CPR are represented by small genomes and cell sizes with restricted metabolic capacities, which might have been inherited from an early metabolic platform for life (Hug et al. 2016).
For the oceanic crust biosphere, the JOIDES Resolution (JR) was used to drill 13, 33.5 and 104 million-year-old basalt lava during Integrated Ocean Drilling Program (IODP) Expedition 329 that targeted life beneath the seafloor of the South Pacific Gyre (SPG). To understand the nature of rocky biosphere in oceanic crust, a new life-detection technique was successfully developed for drilled rock cores in combination with nanoscale mineralogical characterizations (see Yamashita et al. 2019 and Sueoka et al. 2019 for technical details). Basalt fractures filled with clay minerals and calcium carbonate were associated with the formation of Fe/Mg- smectite compositionally and structurally similar to saponite and/or nontronite, indicators of low-temperature basalt-water interactions. Unexpectedly, the dense colonization of microbial cells was directly imaged to exceed ~1010 cells/cm3, a range of cell density typically found in human gut. More surprisingly, the dominance of heterotrophic bacteria was indicated by analyses of DNA sequences and lipids to conclude organic matter as carbon and energy sources in subseafloor basalt.
These findings change our view of the rocky biosphere where inorganic energy sources derived from rock-water interactions are generally regarded as primary ecological importance. Given the prominence of basaltic lava and/or magmatic methane on Earth and Mars, microbial life could be habitable where subsurface igneous rocks interact with liquid water. It is also important to note that microbial presence/absence and metabolic repertories will clarify poorly characterized physicochemical properties in deep igneous rocks such as permeability and fluid and energy fluxes. Finally, the technology is ready to hunt mineral-centered life in the deep subsurface for unveiling the life’s story from the very beginning.
REFERENCES
Hug, L. et al. (2016) Nature Microbiology 1, Article number: 16048.
Ino et al. (2018) ISME Journal 12: 31-47
Yamashita, S. et al. (2019) Scientific Reports 9, Article number 11306.
Sueoka, Y. et al. (2019) Frontiers in Microbiology, doi: 10.3389/fmicb.2019.02793.
Suzuki, Y. et al. (2020) Communications Biology, doi: 10.1038/s42003-020-0860-1.